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Proper migration of lymphatic endothelial cells requires survival and guidance cues from arterial mural cells

The migration of lymphatic endothelial cells (LECs) is key for the development of the complex and vast lymphatic vascular network that pervades most tissues in an organism. In zebrafish, arterial intersegmental vessels together with chemokines have been shown to promote lymphatic cell migration from...

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Autores principales: Peng, Di, Ando, Koji, Hußmann, Melina, Gloger, Marleen, Skoczylas, Renae, Mochizuki, Naoki, Betsholtz, Christer, Fukuhara, Shigetomo, Schulte-Merker, Stefan, Lawson, Nathan D, Koltowska, Katarzyna
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9042226/
https://www.ncbi.nlm.nih.gov/pubmed/35316177
http://dx.doi.org/10.7554/eLife.74094
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author Peng, Di
Ando, Koji
Hußmann, Melina
Gloger, Marleen
Skoczylas, Renae
Mochizuki, Naoki
Betsholtz, Christer
Fukuhara, Shigetomo
Schulte-Merker, Stefan
Lawson, Nathan D
Koltowska, Katarzyna
author_facet Peng, Di
Ando, Koji
Hußmann, Melina
Gloger, Marleen
Skoczylas, Renae
Mochizuki, Naoki
Betsholtz, Christer
Fukuhara, Shigetomo
Schulte-Merker, Stefan
Lawson, Nathan D
Koltowska, Katarzyna
author_sort Peng, Di
collection PubMed
description The migration of lymphatic endothelial cells (LECs) is key for the development of the complex and vast lymphatic vascular network that pervades most tissues in an organism. In zebrafish, arterial intersegmental vessels together with chemokines have been shown to promote lymphatic cell migration from the horizontal myoseptum (HM). We observed that emergence of mural cells around the intersegmental arteries coincides with lymphatic departure from HM which raised the possibility that arterial mural cells promote LEC migration. Our live imaging and cell ablation experiments revealed that LECs migrate slower and fail to establish the lymphatic vascular network in the absence of arterial mural cells. We determined that mural cells are a source for the C-X-C motif chemokine 12 (Cxcl12a and Cxcl12b), vascular endothelial growth factor C (Vegfc) and collagen and calcium-binding EGF domain-containing protein 1 (Ccbe1). We showed that chemokine and growth factor signalling function cooperatively to induce robust LEC migration. Specifically, Vegfc-Vegfr3 signalling, but not chemokines, induces extracellular signal-regulated kinase (ERK) activation in LECs, and has an additional pro-survival role in LECs during the migration. Together, the identification of mural cells as a source for signals that guide LEC migration and survival will be important in the future design for rebuilding lymphatic vessels in disease contexts.
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spelling pubmed-90422262022-04-27 Proper migration of lymphatic endothelial cells requires survival and guidance cues from arterial mural cells Peng, Di Ando, Koji Hußmann, Melina Gloger, Marleen Skoczylas, Renae Mochizuki, Naoki Betsholtz, Christer Fukuhara, Shigetomo Schulte-Merker, Stefan Lawson, Nathan D Koltowska, Katarzyna eLife Developmental Biology The migration of lymphatic endothelial cells (LECs) is key for the development of the complex and vast lymphatic vascular network that pervades most tissues in an organism. In zebrafish, arterial intersegmental vessels together with chemokines have been shown to promote lymphatic cell migration from the horizontal myoseptum (HM). We observed that emergence of mural cells around the intersegmental arteries coincides with lymphatic departure from HM which raised the possibility that arterial mural cells promote LEC migration. Our live imaging and cell ablation experiments revealed that LECs migrate slower and fail to establish the lymphatic vascular network in the absence of arterial mural cells. We determined that mural cells are a source for the C-X-C motif chemokine 12 (Cxcl12a and Cxcl12b), vascular endothelial growth factor C (Vegfc) and collagen and calcium-binding EGF domain-containing protein 1 (Ccbe1). We showed that chemokine and growth factor signalling function cooperatively to induce robust LEC migration. Specifically, Vegfc-Vegfr3 signalling, but not chemokines, induces extracellular signal-regulated kinase (ERK) activation in LECs, and has an additional pro-survival role in LECs during the migration. Together, the identification of mural cells as a source for signals that guide LEC migration and survival will be important in the future design for rebuilding lymphatic vessels in disease contexts. eLife Sciences Publications, Ltd 2022-03-22 /pmc/articles/PMC9042226/ /pubmed/35316177 http://dx.doi.org/10.7554/eLife.74094 Text en © 2022, Peng et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Developmental Biology
Peng, Di
Ando, Koji
Hußmann, Melina
Gloger, Marleen
Skoczylas, Renae
Mochizuki, Naoki
Betsholtz, Christer
Fukuhara, Shigetomo
Schulte-Merker, Stefan
Lawson, Nathan D
Koltowska, Katarzyna
Proper migration of lymphatic endothelial cells requires survival and guidance cues from arterial mural cells
title Proper migration of lymphatic endothelial cells requires survival and guidance cues from arterial mural cells
title_full Proper migration of lymphatic endothelial cells requires survival and guidance cues from arterial mural cells
title_fullStr Proper migration of lymphatic endothelial cells requires survival and guidance cues from arterial mural cells
title_full_unstemmed Proper migration of lymphatic endothelial cells requires survival and guidance cues from arterial mural cells
title_short Proper migration of lymphatic endothelial cells requires survival and guidance cues from arterial mural cells
title_sort proper migration of lymphatic endothelial cells requires survival and guidance cues from arterial mural cells
topic Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9042226/
https://www.ncbi.nlm.nih.gov/pubmed/35316177
http://dx.doi.org/10.7554/eLife.74094
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